Saccadic eye movements minimize the consequences of motor noise

The durations and trajectories of our saccadic eye movements are remarkably stereotyped. We have no voluntary control over these properties but they are determined by the movement amplitude and, to a smaller extent, also by the movement direction and initial eye orientation. Here we show that the stereotyped durations and trajectories are optimal for minimizing the variability in saccade endpoints that is caused by motor noise. The optimal duration can be understood from the nature of the motor noise, which is a combination of signal-dependent noise favoring long durations, and constant noise, which prefers short durations. The different durations of horizontal vs. vertical and of centripetal vs. centrifugal saccades, and the somewhat surprising properties of saccades in oblique directions are also accurately predicted by the principle of minimizing movement variability. The simple and sensible principle of minimizing the consequences of motor noise thus explains the full stereotypy of saccadic eye movements. This suggests that saccades are so stereotyped because that is the best strategy to minimize movement errors for an open-loop motor system.     

The Main Sequence of Saccades Optimizes Speed-accuracy Trade-off

In primates, it is well known that there is a consistent relationship between the duration, peak velocity and amplitude of saccadic eye movements, known as the ‘main sequence’. The reason why such a stereotyped relationship evolved is unknown. We propose that a fundamental constraint on the deployment of foveal vision lies in the motor system that is perturbed by signal-dependent noise (proportional noise) on the motor command. This noise imposes a compromise between the speed and accuracy of an eye movement. We propose that saccade trajectories have evolved to optimize a trade-off between the accuracy and duration of the movement. Taking a semi-analytical approach we use Pontryagin’s minimum principle to show that there is an optimal trajectory for a given amplitude and duration; and that there is an optimal duration for a given amplitude. It follows that the peak velocity is also fixed for a given amplitude. These predictions are in good agreement with observed saccade trajectories and the main sequence. Moreover, this model predicts a small saccadic dead-zone in which it is better to stay eccentric of target than make a saccade onto target. We conclude that the main sequence has evolved as a strategy to optimize the trade-off between accuracy and speed.     

The saccadic and neurological deficits in type 3 Gaucher disease

Our objective was to characterize the saccadic eye movements in patients with type 3 Gaucher disease (chronic neuronopathic) in relationship to neurological and neurophysiological abnormalities. For approximately 4 years, we prospectively followed a cohort of 15 patients with Gaucher type 3, ages 8-28 years, by measuring saccadic eye movements using the scleral search coil method. We found that patients with type 3 Gaucher disease had a significantly higher regression slope of duration vs amplitude and peak duration vs amplitude compared to healthy controls for both horizontal and vertical saccades. Saccadic latency was significantly increased for horizontal saccades only. Downward saccades were more affected than upward saccades. Saccade abnormalities increased over time in some patients reflecting the slowly progressive nature of the disease. Phase plane plots showed individually characteristic patterns of abnormal saccade trajectories. Oculo-manual dexterity scores on the Purdue Pegboard test were low in virtually all patients, even in those with normal cognitive function. Vertical saccade peak duration vs amplitude slope significantly correlated with IQ and with the performance on the Purdue Pegboard but not with the brainstem and somatosensory evoked potentials. We conclude that, in patients with Gaucher disease type 3, saccadic eye movements and oculo-manual dexterity are representative neurological functions for longitudinal studies and can probably be used as endpoints for therapeutic clinical trials. TRIAL REGISTRATION: ClinicalTrials.gov NCT00001289.     

Probability of Seeing Increases Saccadic Readiness

Associating movement directions or endpoints with monetary rewards or costs influences movement parameters in humans, and associating movement directions or endpoints with food reward influences movement parameters in non-human primates. Rewarded movements are facilitated relative to non-rewarded movements. The present study examined to what extent successful foveation facilitated saccadic eye movement behavior, with the hypothesis that foveation may constitute an informational reward. Human adults performed saccades to peripheral targets that either remained visible after saccade completion or were extinguished, preventing visual feedback. Saccades to targets that were systematically extinguished were slower and easier to inhibit than saccades to targets that afforded successful foveation, and this effect was modulated by the probability of successful foveation. These results suggest that successful foveation facilitates behavior, and that obtaining the expected sensory consequences of a saccadic eye movement may serve as a reward for the oculomotor system.     

Saccadic head movements of the praying mantis, with particular reference to visual and proprioceptive information

ABSTRACT. Horizontal head movements of the praying mantis, Sphodromantis lineola Burm., were recorded continuously. They responded to the presence of a live blowfly prey in the antero-lateral visual field with a rapid saccadic head movement. The angular movement of a fixation saccade was correlated positively to the displacement of the prey from the prothoracic midline. Saccade magnitude and velocity are related. After the stimulus moved out of the visual field, the mantis made a second saccadic head movement, a return saccade towards the body midline. We observed return saccades in which the head overshot or undershot the body midline, as well as saccades which returned the head exactly to its initial position. In 92% of trials with intact mantids, the return movement succeeded eventually in rotating the head back to its initial position, whereas after removal of the neck hair plates this occurred in only 47% of trials. There is a consistent relation between saccade extent and velocity. Velocities of return saccades were slower than those of fixation saccades. It is suggested that sensory inputs from the neck hair plate proprioceptors modify both the magnitude and the angular velocity of fixation and return saccadic head movements.     

Both Lexical and Non-Lexical Characters Are Processed during Saccadic Eye Movements

On average our eyes make 3–5 saccadic movements per second when we read, although their neural mechanism is still unclear. It is generally thought that saccades help redirect the retinal fovea to specific characters and words but that actual discrimination of information only occurs during periods of fixation. Indeed, it has been proposed that there is active and selective suppression of information processing during saccades to avoid experience of blurring due to the high-speed movement. Here, using a paradigm where a string of either lexical (Chinese) or non-lexical (alphabetic) characters are triggered by saccadic eye movements, we show that subjects can discriminate both while making saccadic eye movement. Moreover, discrimination accuracy is significantly better for characters scanned during the saccadic movement to a fixation point than those not scanned beyond it. Our results showed that character information can be processed during the saccade, therefore saccades during reading not only function to redirect the fovea to fixate the next character or word but allow pre-processing of information from the ones adjacent to the fixation locations to help target the next most salient one. In this way saccades can not only promote continuity in reading words but also actively facilitate reading comprehension.     

Blink Perturbation Effects on Saccades Evoked by Microstimulation of the Superior Colliculus

Current knowledge of saccade-blink interactions suggests that blinks have paradoxical effects on saccade generation. Blinks suppress saccade generation by attenuating the oculomotor drive command in structures like the superior colliculus (SC), but they also disinhibit the saccadic system by removing the potent inhibition of pontine omnipause neurons (OPNs). To better characterize these effects, we evoked the trigeminal blink reflex by delivering an air puff to one eye as saccades were evoked by sub-optimal stimulation of the SC. For every stimulation site, the peak and average velocities of stimulation with blink movements (SwBMs) were lower than stimulation-only saccades (SoMs), supporting the notion that the oculomotor drive is weakened in the presence of a blink. In contrast, the duration of the SwBMs was longer, consistent with the hypothesis that the blink-induced inhibition of the OPNs could prolong the window of time available for oculomotor commands to drive an eye movement. The amplitude of the SwBM could also be larger than the SoM amplitude obtained from the same site, particularly for cases in which blink-associated eye movements exhibited the slowest kinematics. The results are interpreted in terms of neural signatures of saccade-blink interactions.     

Computer simulation of overshoot in saccadic eye movements.

The human horizontal eye movement system produces quick, precise, conjugate eye movements called saccades. These are important in normal vision. For example, reading tasks exclusively utilize saccadic eye movements. The majority of saccades have dynamic overshoot. The amplitude of this overshoot is independent of saccadic amplitude, and is such that it places the image of the stimulus within the retinal region of maximum acuity within a minimum of time. A computer based model of the saccadic mechanisms was used to study the origin of this overshoot. It was discussed that dynamic overshoot cannot be attributed to biomechanism properites of the eye movement mechanism, but must instead be explained by variations in the controlling nervous activity. The form of this neural controller signal is very similar to that required for a time optimal response of an inertial system.     

Saccadic adaptation to moving targets

Saccades are so called ballistic movements which are executed without online visual feedback. After each saccade the saccadic motor plan is modified in response to post-saccadic feedback with the mechanism of saccadic adaptation. The post-saccadic feedback is provided by the retinal position of the target after the saccade. If the target moves after the saccade, gaze may follow the moving target. In that case, the eyes are controlled by the pursuit system, a system that controls smooth eye movements. Although these two systems have in the past been considered as mostly independent, recent lines of research point towards many interactions between them. We were interested in the question if saccade amplitude adaptation is induced when the target moves smoothly after the saccade. Prior studies of saccadic adaptation have considered intra-saccadic target steps as learning signals. In the present study, the intra-saccadic target step of the McLaughlin paradigm of saccadic adaptation was replaced by target movement, and a post-saccadic pursuit of the target. We found that saccadic adaptation occurred in this situation, a further indication of an interaction of the saccadic system and the pursuit system with the aim of optimized eye movements.     

Human fast negative EEG potentials before express saccades

Fast negative EEG potentials preceding fast regular saccades and express saccades were studied by the method of backward averaging under conditions of monocular stimulation of the right and left eye. "Step" and "gap" experimental paradigms were used for visual stimulation. Analysis of parameters of potentials and their spatiotemporal dynamics suggests that, under conditions of the increased attention and optimal readiness of the neural structures, express saccades appear when the previously chosen program of the future eye movement coincides with the actual target coordinates. We assumed that the saccade latency decreases at the expense of the involvement of the main oculomotor areas of motor and saccadic planning in its initiation; an express saccade can be initiated also by means of direct transmission of the signal from the cortex to the brainstem saccadic generator passing by the superior colliculus. Moreover, anticipating release from the central fixation and attention distraction are necessary for the successful initiation of an express saccade.     

A model of the saccade-generating system that accounts for trajectory variations produced by competing visual stimuli

Variable saccade trajectories are produced in visual search paradigms in which multiple potential target stimuli are present. These variable trajectories provide a rich source of information that may lead to a deeper understanding of the basic control mechanisms of the saccadic system. We have used published behavioral observations and neural recordings in the superior colliculus (SC), gathered in monkeys performing visual search paradigms, to guide the construction of a new distributed model of the saccadic system. The new model can account for many of the variations in saccade trajectory produced by the appearance of multiple visual stimuli in a search paradigm. The model uses distributed feedback about current eye motion from the brainstem to the SC to reduce activity there at physiologically realistic rates during saccades. The long-range lateral inhibitory connections between SC cells used in previous models have been eliminated to match recent physiological evidence. The model features interactions between visually activated multiple populations of cells in the SC and distributed and topologically organized inhibitory input to the SC from the SNr to produce some of the types of variable saccadic trajectories, including slightly curved and averaging saccades, observed in visual search tasks. The distributed perisaccadic disinhibition of SC from the substantia nigra (SNr) is assumed to have broad spatial tuning. In order to produce the strongly curved saccades occasionally recorded in visual search, the existence of a parallel input to the saccadic burst generators in addition to that provided by the distributed input from the SC is required. The spatiotemporal form of this additional parallel input is computed based on the assumption that the input from the model SC is realistic. In accordance with other recent models, it is assumed that the parallel input comes from the cerebellum, but our model predicts that the parallel input is delayed during highly curved saccadic trajectories.     

A competitive integration model of exogenous and endogenous eye movements

We present a model of the eye movement system in which the programming of an eye movement is the result of the competitive integration of information in the superior colliculi (SC). This brain area receives input from occipital cortex, the frontal eye fields, and the dorsolateral prefrontal cortex, on the basis of which it computes the location of the next saccadic target. Two critical assumptions in the model are that cortical inputs are not only excitatory, but can also inhibit saccades to specific locations, and that the SC continue to influence the trajectory of a saccade while it is being executed. With these assumptions, we account for many neurophysiological and behavioral findings from eye movement research. Interactions within the saccade map are shown to account for effects of distractors on saccadic reaction time (SRT) and saccade trajectory, including the global effect and oculomotor capture. In addition, the model accounts for express saccades, the gap effect, saccadic reaction times for antisaccades, and recorded responses from neurons in the SC and frontal eye fields in these tasks.     

Looking for Discriminating Is Different from Looking for Looking’s Sake

Recent studies provide evidence for task-specific influences on saccadic eye movements. For instance, saccades exhibit higher peak velocity when the task requires coordinating eye and hand movements. The current study shows that the need to process task-relevant visual information at the saccade endpoint can be, in itself, sufficient to cause such effects. In this study, participants performed a visual discrimination task which required a saccade for successful completion. We compared the characteristics of these task-related saccades to those of classical target-elicited saccades, which required participants to fixate a visual target without performing a discrimination task. The results show that task-related saccades are faster and initiated earlier than target-elicited saccades. Differences between both saccade types are also noted in their saccade reaction time distributions and their main sequences, i.e., the relationship between saccade velocity, duration, and amplitude.     

The effect of saccades on threshold perception — A model study

The effect of saccadic eye movements on threshold perception is investigated theoretically. The proposed model considers eye movements by taking into account the shifting of the stimulus pattern on the retina during the occurrence of an eye movement. Saccades are characterized by high velocity and short duration. These motions cause overshoots in the response of linear filters to certain stimulus patterns. Therefore, the model predicts facilitation effects of saccades in the perception of low spatial frequency patterns and patterns flickering with high temporal frequencies. These results agree with experimentally obtained data presented in a subsequent paper. A simple approach is formulated which approximates the complex shifting function of a saccade by a switching of the pattern.     

Dysfunctional mode switching between fixation and saccades: collaborative insights into two unusual clinical disorders

Voluntary rapid eye movements (saccades) redirect the fovea toward objects of visual interest. The saccadic system can be considered as a dual-mode system: in one mode the eye is fixating, in the other it is making a saccade. In this review, we consider two examples of dysfunctional saccades, interrupted saccades in late-onset Tay-Sachs disease and gaze-position dependent opsoclonus after concussion, which fail to properly shift between fixation and saccade modes. Insights and benefits gained from bi-directional collaborative exchange between clinical and basic scientists are emphasized. In the case of interrupted saccades, existing mathematical models were sufficiently detailed to provide support for the cause of interrupted saccades. In the case of gaze-position dependent opsoclonus, existing models could not explain the behavior, but further development provided a reasonable hypothesis for the mechanism underlying the behavior. Collaboration between clinical and basic science is a rich source of progress for developing biologically plausible models and understanding neurological disease. Approaching a clinical problem with a specific hypothesis (model) in mind often prompts new experimental tests and provides insights into basic mechanisms.

     

Effect of dopamine deficiency on the preparation of visually guided saccadic eye movements

Parameters of saccadic eye movements were studied in patients with Parkinson's disease and control subjects. In parkinsonian patients, the number of slow regular saccades was shown to be increased, and the number of express saccades was shown to be decreased. As a result the mean of saccade latency in patients was longer than in the control group. Moreover, the percentage of multistep saccades in patients with Parkinson's disease. In this case, not one but two or three saccades were performed with smaller amplitude to the target. We point, that the multistep saccades occurred mainly among the express saccades. Obviously, the dopamine deficiency distinguishing parkinsonian patients takes the primary part in the development of saccadic disorders. Degeneration of the nigrostriatal dopamine pathway results in imbalance in activity of the direct and indirect output pathways of the striatum. We suppose that this leads to inhibition of neurons activity in the superior colliculus during the saccade performance, which results in the early saccade interruption. In support of this reasoning, the mean of saccade latency and the percentage of the multistep saccades decreased in patients with Parkinson's disease after dopamine D2/D3 agonist (piribedil) treatment, due to activity restoration of the indirect pathway.     

Evidence for the lateral intraparietal area as the parietal eye field.

It has long been appreciated that the posterior parietal cortex plays a role in the processing of saccadic eye movements. Only recently has it been discovered that a small cortical area, the lateral intraparietal area, within this much larger area appears to be specialized for saccadic eye movements. Unlike other cortical areas in the posterior parietal cortex, the lateral intraparietal area has strong anatomical connections to other saccade centers, and its cells have saccade-related responses that begin before the saccades. The lateral intraparietal area appears to be neither a strictly visual nor strictly motor structure; rather it performs visuomotor integration functions including determining the spatial location of saccade targets and forming plans to make eye movements.     

Cognitive Control of Saccadic Eye Movements in Children with Developmental Coordination Disorder

The ability to use advance information to prepare and execute a movement requires cognitive control of behaviour (e.g., anticipation and inhibition). Our aim was to explore the integrity of saccadic eye movement control in developmental coordination disorder (DCD) and typically developing (TD) children (8–12 years) and assess how these children plan and inhibit saccadic responses, the principal mechanisms within visual attention control. Eye movements and touch responses were measured (separately and concurrently) in Cued and Non-Cued conditions. We found that children with DCD had similar saccade kinematics to the TD group during saccade initiation. Advance information decreased hand movement duration in both groups during Cued trials, but decrements in accuracy were significantly worse in the DCD group. In addition, children with DCD exhibited greater inhibitory errors and inaccurate fixation during the Cued trials. Thus, children with DCD were reasonably proficient in executing saccades during reflexive (Non-Cued) conditions, but showed deficits in more complex control processes involving prediction and inhibition. These findings have implications for our understanding of motor control in children with DCD.     

The Human Frontal Oculomotor Cortical Areas Contribute Asymmetrically to Motor Planning in a Gap Saccade Task

Background

Saccadic eye movements are used to rapidly align the fovea with the image of objects of interest in peripheral vision. We have recently shown that in children there is a high preponderance of quick latency but poorly planned saccades that consistently fall short of the target goal. The characteristics of these multiple saccades are consistent with a lack of proper inhibitory control of cortical oculomotor areas on the brainstem saccade generation circuitry.

Methodology/Principal Findings

In the present paper, we directly tested this assumption by using single pulse transcranial magnetic stimulation (TMS) to transiently disrupt neuronal activity in the frontal eye fields (FEF) and supplementary eye fields (SEF) in adults performing a gap saccade task. The results showed that the incidence of multiple saccades was increased for ispiversive but not contraversive directions for the right and left FEF, the left SEF, but not for the right SEF. Moreover, this disruption was most substantial during the ∼50 ms period around the appearance of the peripheral target. A control condition in which the dorsal motor cortex was stimulated demonstrated that this was not due to any non-specific effects of the TMS influencing the spatial distribution of attention.

Conclusions/Significance

Taken together, the results are consistent with a direction-dependent role of the FEF and left SEF in delaying the release of saccadic eye movements until they have been fully planned.     

Differentiation between vergence and saccadic functional activity within the human frontal eye fields and midbrain revealed through fMRI

Purpose

Eye movement research has traditionally studied solely saccade and/or vergence eye movements by isolating these systems within a laboratory setting. While the neural correlates of saccadic eye movements are established, few studies have quantified the functional activity of vergence eye movements using fMRI. This study mapped the neural substrates of vergence eye movements and compared them to saccades to elucidate the spatial commonality and differentiation between these systems.

Methodology

The stimulus was presented in a block design where the ‘off’ stimulus was a sustained fixation and the ‘on’ stimulus was random vergence or saccadic eye movements. Data were collected with a 3T scanner. A general linear model (GLM) was used in conjunction with cluster size to determine significantly active regions. A paired t-test of the GLM beta weight coefficients was computed between the saccade and vergence functional activities to test the hypothesis that vergence and saccadic stimulation would have spatial differentiation in addition to shared neural substrates.

Results

Segregated functional activation was observed within the frontal eye fields where a portion of the functional activity from the vergence task was located anterior to the saccadic functional activity (z>2.3; p<0.03). An area within the midbrain was significantly correlated with the experimental design for the vergence but not the saccade data set. Similar functional activation was observed within the following regions of interest: the supplementary eye field, dorsolateral prefrontal cortex, ventral lateral prefrontal cortex, lateral intraparietal area, cuneus, precuneus, anterior and posterior cingulates, and cerebellar vermis. The functional activity from these regions was not different between the vergence and saccade data sets assessed by analyzing the beta weights of the paired t-test (p>0.2).

Conclusion

Functional MRI can elucidate the differences between the vergence and saccade neural substrates within the frontal eye fields and midbrain.